Geographic variation in density, demography, and life history traits of a harvested temperate sex-changing reef fish

Description

Geographic variation in ecological and environmental factors may lead to intraspecific differences among populations. For the California sheephead (Semicossyphus pulcher), an important predator in kelp forests and a target of commercial and recreational fisheries, we evaluated the degree to which different populations exhibited variation in density, demography, and life history traits. We assessed biogeographic patterns of abundance through underwater visual census at 39 sites spanning a major portion of the species range (southern California, USA, to Baja California, Mexico) and made collections from seven focal sites to investigate geographic differences in demography and life histories. California sheephead densities were significantly greater in the southern part of their range and at offshore islands than along the mainland coast. At the focal sites, we found significant spatial variation in density, fecundity, size structure, growth rates, annual survivorship, and the timing of maturation and sex change. Density- and temperature-dependent effects helped to explain the intraspecific differences in these parameters. Studies such as this one will allow for demographic plasticity to be incorporated into future stock assessments. Management of temperate reef fishes may best be achieved on smaller spatial scales as we increase our understanding of geographic variation among populations.

Spatial and temporal variation in the natal otolith chemistry of a Hawaiian reef fish: Prospects for measuring population connectivity,

Description

, , , One of the most compelling unanswered questions in marine ecology is the extent to which local populations are connected via larval exchange. Recent work has suggested that variation in the chemistry of otoliths (earstones) of fishes may function as a natural tag, potentially allowing investigators to determine sources of individual larvae and estimate larval connectivity. We analyzed the spatial and temporal variation in natal otolith chemistry of a benthic-spawning reef fish from the Hawaiian Islands. We found no consistent chemical variation at the largest scale (>100 km, among islands), but found significant variation at moderate scales (sites within islands, tens of kilometres) and small scales (clutches within sites), and chemistry of otoliths was not stable between years. These results imply that we may be able to use otolith chemistry to track larval dispersal only if the scales of dispersal match those of variation in natal otolith chemistry, and that separate natal otolith collections may be needed to track different cohorts of larvae. Finally, we found that elemental composition of recruit cores often did not match that of natal otoliths, suggesting that additional methodological development is required before we can effectively apply methods in otolith chemistry to the study of larval dispersal., ,

Elevated levels of trace elements in cores of otoliths and their potential for use as natural tags,

Description

, , , Variation in the chemical composition of fish otoliths has been used in recent years to
address a range of ecological questions, including levels of stock mixing, variation in habitat use, and
rates of larval exchange. While some of these questions have been answered with varying success,
the degree to which discrete populations are connected via larval exchange remains unknown. To
identify larval sources using natural variation in otolith chemistry, we must distinguish and measure
the chemical composition of the otolith core, the portion of the otolith formed at the spawning site.
Using laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS), we found that the
core regions of otoliths from 6 different species of fishes were highly enriched in manganese (Mn),
and elevated in magnesium (Mg) and barium (Ba), relative to adjacent regions of the otolith. These
patterns were consistent for species drawn from different taxonomic groups, which inhabit temperate
and tropical regions, are found in marine and freshwater, and utilize a variety of spawning modes.
Variation among species in Mn concentration in the core also corresponds to maternal investment,
measured by egg size. These data suggest that core enrichment may be a general characteristic of
otoliths, and that the chemical composition of the otolith core is fundamentally different from other
regions of the otolith. The localized elemental enrichment of the core underscores the importance of
methods that analyze the core region in small, discrete samples if otolith chemistry is used to address
questions of larval exchange among populations., ,

, , , There is a growing realization that the scale and degree of population connectivity are crucial to the dynamics and persistence of spatially structured populations. For marine organisms with complex life cycles, experiences during larval life may influence phenotypic traits, performance, and the probability of postsettlement survival. For a Caribbean reef fish (Thalassoma bifasciatum) on an oceanic island, we used otolith (ear stone) elemental profiles of lead (Pb) to assign recent settlers to a group that developed in waters elevated in Pb concentrations throughout larval life (i.e., nearshore signature) and a group that developed in waters depleted in Pb (i.e., offshore signature), potentially dispersing from upstream sources across oceanic waters. Larval history influenced early life history traits: offshore developers initially grew slowly but compensated with fast growth upon entering nearshore waters and metamorphosed in better condition with higher energy reserves. As shown in previous studies, local production contributed heavily to settlement: at least 45% of settlers developed nearshore. However, only 23% of survivors after the first month displayed a nearshore otolith profile. Therefore, settlers with different larval histories suffered differential mortality. Importantly, selective mortality was mediated by larval history, in that the postsettlement intensity of selection was much greater for fish that developed nearshore, potentially because they had developed in a less selectively intense larval environment. Given the potential for asymmetrical postsettlement source-based survival, successful spatial management of marine populations may require knowledge of “realized connectivity” on ecological scales, which takes into account the postsettlement fitness of individuals from different sources., ,

Geographic variation in natal and early larval trace-elemental signatures in the statoliths of the market squid Doryteuthis (formerly Loligo) opalescens,

Description

, , , We found distinct geographic differences in trace element concentrations in both the core and early larval areas of the statoliths of paralarval market squid Doryteuthis (= Loligo) opalescens at sites throughout the Southern California Bight, USA. Laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS) of individual statoliths indicated detectable levels of Mg, Mn, Sr, and Ba, with marginal levels of Cr and Pb. While these paralarvae showed considerable within-sample differences in elemental concentrations, there was significant between-site discrimination of natal (core) and early larval signatures for collection sites up to 100 km apart. In 2002 and 2003, levels of Ba and Sr in the statolith cores were significantly different among sites, suggesting differences in the natal environment or local maternal effects. Site specific differences in elemental signatures were also apparent for Mg and Mn in samples taken from outside the core in the early post-hatching period. These same portions of the statolith can be analyzed from adult squid collected on spawning grounds. We showed that concentrations of trace elements in the statolith cores of adults closely resembled the core signatures of squid paralarvae, which opens the possibility of identifying the source populations for stocks of this commercially important species., ,

The interaction of retention, recruitment, and density-dependent mortality in the spatial placement of marine reserves,

Description

Population density can affect rates of mortality and individual growth. We measured these for the nonexploited bluehead wrasse, Thalassoma bifasciatum, at three sites around St. Croix, US Virgin Islands. Previous work demonstrated that differences in the degree of larval retention in these sites results in very large differences in recruitment intensity. Post-settlement mortality differed among sites and was positively related to recruitment density. Post-settlement growth differences were small. Because of strong mortality effects early in life, adult densities and size/age distributions differed among sites and did not reflect differences in recruitment rate. The site with the highest retention and recruitment (Butler Bay) had many small fish, while the two other sites with lower recruitment rates (Jacks Bay and Green Cay) had proportionally more large fish. These differences resulted in large differences in egg production. Per capita production was highest at the lowest density site (Green Cay).
Total egg production at Green Cay was 75% that at Butler Bay, despite only having half the population size, and the highest overall production was at Jacks Bay, with low retention and moderate recruitment. In terms of marine reserve location, sites predicted to have high retention and recruitment may not always be the sites of highest egg production due to density-dependent processes, and it is important to consider the relative values of self-recruitment and larval export in reserve design., , ,

Exploitation and recovery of a sea urchin predator has implications for the resilience of southern California kelp forests

Description

Size-structured predator–prey interactions can be altered by the history of exploitation, if that exploitation is itself size-selective. For example, selective harvesting of larger sized predators can release prey populations in cases where only large individuals are capable of consuming a particular prey species. In this study, we examined how the history of exploitation and recovery (inside marine reserves and due to fisheries management) of California sheephead (Semicossyphus pulcher) has affected size-structured interactions with sea urchin prey in southern California. We show that fishing changes size structure by reducing sizes and alters life histories of sheephead, while management measures that lessen or remove fishing impacts (e.g. marine reserves, effort restrictions) reverse these effects and result in increases in density, size and biomass. We show that predation on sea urchins is size-dependent, such that the diet of larger sheephead is composed of more and larger sized urchins than the diet of smaller fish. These results have implications for kelp forest resilience, because urchins can overgraze kelp in the absence of top-down control. From surveys in a network of marine reserves, we report negative relationships between the abundance of sheephead and urchins and the abundance of urchins and fleshy macroalgae (including giant kelp), indicating the potential for cascading indirect positive effects of top predators on the abundance of primary producers. Management measures such as increased minimum size limits and marine reserves may serve to restore historical trophic roles of key predators and thereby enhance the resilience of marine ecosystems.

Fecundity estimates used in a 2004 stock assessment to evaluate the overall health of the population of California sheephead Semicossyphus pulcher were based primarily on two studies. The first estimated the total fecundity of only nine individuals captured near Santa Catalina Island, California, and the second estimated batch fecundity of individuals taken from only one artificial reef. In order to develop a current and more comprehensive estimate of fecundity, we collected California sheephead from seven locations off southern California throughout the spawning season (July through September). To estimate both total fecundity and batch fecundity, we categorized and counted oocytes from ovarian subsamples of 28 and 24 (respectively) mature females (stage 3, spawning capable; determined by histological analysis). Total and batch fecundity increased with somatic mass, standard length, and ovary mass. We found total fecundity to increase with somatic mass to a power of 5.5, which is considerably greater than the value
(2.95) reported previously. Our observations therefore highlight the importance of large females in the reproductive potential of the California sheephead stock. Regression analysis indicates that ovary mass is the most accurate biological indicator of fecundity for California sheephead and should be used for subsequent stock analyses., , ,

Size-selective harvesting alters life histories of a temperate sex-changing fish,

Description

, , , Selective mortality, whether caused naturally by predation or through the
influence of harvest practices, initiates changes within populations when individuals possessing
certain heritable traits have increased fitness. Theory predicts that increased mortality rates
will select for changes in a number of different life history characteristics. For example, fishing
often targets larger individuals and has been shown repeatedly to alter population size
structure and growth rates, and the timing of maturation. For sex-changing species, selective
fishing practices can affect additional traits such as the mature population sex ratio and the
timing of sexual transformation. Using historical comparisons, we examined the effects of
exploitation on life history characteristics of California sheephead, Semicossyphus pulcher, a
temperate protogynous (female–male sex changer) labrid that inhabits nearshore rocky
environments from central California, USA, to southern Baja California, Mexico.
Recreational fishing intensified and an unregulated commercial live-fish fishery developed
rapidly in southern California between the historical and current studies. Collections of S.
pulcher from three locations (Bahı´a Tortugas, Catalina Island, and San Nicolas Island) in 1998
were compared with data collected 20–30 years previously to ascertain fishery-induced changes
in life history traits. At Bahı´a Tortugas, where fishing by the artisanal community remained
light and annual survivorship stayed high, we observed no changes in size structure or shifts in
the timing of maturation or the timing of sex change. In contrast, where recreational
(Catalina) and commercial (San Nicolas) fishing intensified and annual survivorship
correspondingly declined, males and females shifted significantly to smaller body sizes,
females matured earlier and changed sex into males at both smaller sizes and younger ages and
appeared to have a reduced maximum lifespan. Mature sex ratios (female : male) increased at
San Nicolas, despite a twofold reduction in the mean time spent as a mature female. Proper
fisheries management requires measures to prevent sex ratio skew, sperm limitation, and
reproductive failure because populations of sequential hermaphrodites are more sensitive to
size-selective harvest than separate-sex species. This is especially true for S. pulcher, where
different segments of the fishery (commercial vs. recreational) selectively target distinct sizes
and therefore sexes in different locations., ,

, , , Coral and rocky reef fish populations are widely used as model systems for the
experimental exploration of density-dependent vital rates, but patterns of density-dependent
mortality in these systems are not yet fully understood. In particular, the paradigm for strong,
directly density-dependent (DDD) postsettlement mortality stands in contrast to recent
evidence for inversely density-dependent (IDD) mortality. We review the processes responsible
for DDD and IDD per capita mortality in reef fishes, noting that the pattern observed depends
on predator and prey behavior, the spatial configuration of the reef habitat, and the spatial
and temporal scales of observation. Specifically, predators tend to produce DDD prey
mortality at their characteristic spatial scale of foraging, but prey mortality is IDD at smaller
spatial scales due to attack-abatement effects (e.g., risk dilution). As a result, DDD mortality
may be more common than IDD mortality on patch reefs, which tend to constrain predator
foraging to the same scale as prey aggregation, eliminating attack-abatement effects.
Additionally, adjacent groups of prey on continuous reefs may share a subset of refuges,
increasing per capita refuge availability and relaxing DDD mortality relative to prey on patch
reefs, where the patch edge could prevent such refuge sharing. These hypotheses lead to a
synthetic framework to predict expected mortality patterns for a variety of scenarios. For
nonsocial, nonaggregating species and species that aggregate in order to take advantage of
spatially clumped refuges, IDD mortality is possible but likely superseded by DDD refuge
competition, especially on patch reefs. By contrast, for species that aggregate socially,
mortality should be IDD at the scale of individual aggregations but DDD at larger scales. The
results of nearly all prior reef fish studies fit within this framework, although additional work
is needed to test many of the predicted outcomes. This synthesis reconciles some apparent
contradictions in the recent reef fish literature and suggests the importance of accounting for
the scale-sensitive details of predator and prey behavior in any study system., ,

Consistent long-term spatial gradients in replenishment for an island population of a coral reef fish

Description

The population replenishment of marine organisms is routinely characterized as highly
variable and unpredictable in space and time. Using island-wide recruitment surveys of a common
coral reef fish, the bluehead wrasse Thalassoma bifasciatum, in 6 summers spanning a 12 yr period
(1991 to 2003), we examined whether spatial patterns of recruitment are consistent or variable
through time on St. Croix, US Virgin Islands. Despite annual fluctuations in the magnitude of replenishment,
recruitment intensity follows a distinct and consistent spatial gradient that differs in direction
between the north (leeward) and south (windward) shores; recruitment declines from west to
east on the north shore and east to west on the south shore. The rank ordering of sites on each shore
was concordant when recruitment was either pooled across years (monthly variation) or pooled
across months (annual variation). When the 2 highest recruitment sites on each shore were considered
alone, consistent seasonal effects were also apparent, with higher recruitment from June
through August on the north shore, and higher recruitment in September on the south shore. Thus,
while the magnitude of recruitment is indeed variable in space and time, its qualitative pattern is predictable
in this area. Results of prior investigations of larval dispersal and coastal oceanography
around St. Croix shed light on the origin of the consistent recruitment patterns documented in this
study. The potential for consistent spatial and temporal patterns in recruitment is an important consideration
in the spatial management of marine resources.

Otolith barium profiles verify the timing of settlement in a coral reef fish,

Description

, , , Otolith microstructure has been shown to record valuable information about fishes including age, growth, and the timing of life history transitions, while microchemical analysis can reveal information about environmental history, dispersal, and migration. For the bluehead wrasse Thalassoma bifasciatum, a common coral reef fish on an oceanic island, we examined whether otolith chemistry could be used to identify the timing of settlement from the pelagic larval phase to the reef-based juvenile phase. This species has a distinct settlement mark visible in its otolith microstructure. Using laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS), we found that Ba:Ca ratios increased abruptly at the time of settlement. On average, Ba:Ca ratios were 6.5× greater in the juvenile than the larval phase. Other elements (Mg, Mn, and Sr) also displayed ontogenetic changes in concentration; however, those changes were not associated with the settlement mark. We demonstrate the potential utility of otolith chemistry as a method to identify the timing of settlement (and thereby the larval duration) in other marine fishes with similar early life histories, whose otoliths may not produce distinct settlement checks or those whose settlement stage larvae may not be captured by other means., ,

Larval history influences post-metamorphic condition in a coral-reef fish

Description

Upon settlement, many Wshes undergo an energetically costly metamorphic period that requires substantial nutritional reserves. Larval growth and the accumulation of lipids prior to metamorphosis are likely to infuence growth and survival following this critical period. On the Caribbean island of St. Croix, I investigated relationships between larval growth, early life-history characteristics, and post-metamorphic lipid content in the bluehead wrasse Thalassoma bifasciatum. Lipid reserves remaining after metamorphosis were positively related (r2 = 0.62) to the width of the metamorphic band; thus, this otolith-derived trait may be used to estimate the condition at emergence of survivors collected at some later time. In contrast, pelagic larval duration, average larval growth, and otolith size at settlement were negatively related to postmetamorphic lipid content. Interestingly, the trend for slower growth among fish in good condition was not consistent over the entire pelagic larval duration. Analyses of daily larval growth histories indicated that Wsh with high lipid reserves grew rapidly in the last week prior to settlement, but relatively slowly during the early phases of larval life; those emerging with low lipid concentrations, however, displayed strikingly opposite patterns. These contrasting patterns of growth and energy storage were consistent at two sites and over three recruitment events. Otolith chemistry data suggested that diVerences in growth histories and body condition were consistent with the hypothesis
of larval development in distinct oceanic environments (characterized by Pb concentration); but, within a water mass, differences reflected life-history trade-offs between growth and energy storage. The results have implications for understanding the processes driving juvenile survival, which may be condition dependent.

, , , Networks of marine reserves are increasingly a major component of many ecosystem-based management plans designed to conserve biodiversity, protect the structure and function of ecosystems, and rebuild and sustain fisheries. There is a growing need for scientific guidance in the design of network-wide monitoring programs to evaluate the efficacy of reserves at meeting their conservation and
management goals. Here, we present an evaluation of the Channel Islands reserve network, whichwas established in 2003 off the coast of southern California. This reserve network spans a major environmental and biogeographic gradient, making it a challenge to assess network-wide responses of many species. Using fish community structure data from a long-term, large-scale monitoring program,
we first identified persistent geographic patterns of community structure and the scale at which sites should be grouped for analysis. Fish communities differedmost among islandswith densities of individual
species varying from 3- to 250-fold. Habitat structure differed among islands but not based on reserve status. Across the network, we found that, after 5 years, species targeted by fishing had higher densities (1.5×) and biomass (1.8×) inside reserves, whereas nontargeted species showed no significant differences. Examining trophic groups, piscivore and carnivore biomass was significantly greater
inside reserves (1.8× and 1.3× more, respectively), whereas the biomass of planktivores and herbivores was similar inside and out. A framework for incorporating biogeographic variation into reserve
network assessments is critical as we move from the evaluation of single reserves to networks of reserves., ,